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Mixing Genetically and Morphologically Distinct

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Mixing Genetically and Morphologically Distinct Article Mixing Genetically and Morphologically Distinct Populations in Translocations: Asymmetrical Introgression in A Newly Established Population of the Boodie (Bettongia lesueur) Rujiporn Thavornkanlapachai 1,*, Harriet R. Mills 2, Kym Ottewell 3, Judy Dunlop 4,5, Colleen Sims 5, Keith Morris 5, Felicity Donaldson 6 and W. Jason Kennington 1 1 School of Biological Sciences, The University of Western Australia, Crawley, Western Australia 6009, Australia; [email protected] 2 Centre for Ecosystem Management, School of Science, Edith Cowan University, Joondalup, Western Australia 6027, Australia; [email protected] 3 Department of Biodiversity, Conservation and Attractions, Locked Bag 104, Bentley Delivery Centre, Western Australia 6152, Australia; [email protected] 4 School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, Western Australia 6150, Australia; [email protected] 5 Department of Biodiversity, Conservation and Attractions, PO Box 51, Wanneroo, Western Australia 6946, Australia [email protected] (C.S.); [email protected] (K.M.) 6 360 Environmental, 10 Bermondsey Street, West Leederville, Western Australia 6007, Australia; [email protected] * Correspondence: [email protected]; Tel.: +61 8 9219 9089 Received: 22 August 2019; Accepted: 17 September 2019; Published: 19 September 2019 Abstract: The use of multiple source populations provides a way to maximise genetic variation and reduce the impacts of inbreeding depression in newly established translocated populations. However, there is a risk that individuals from different source populations will not interbreed, leading to population structure and smaller effective population sizes than expected. Here, we investigate the genetic consequences of mixing two isolated, morphologically distinct island populations of boodies (Bettongia lesueur) in a translocation to mainland Australia over three generations. Using 18 microsatellite loci and the mitochondrial D-loop region, we monitored the released animals and their offspring between 2010 and 2013. Despite high levels of divergence between the two source populations (FST = 0.42 and ϕST = 0.72), there was clear evidence of interbreeding between animals from different populations. However, interbreeding was non- random, with a significant bias towards crosses between the genetically smaller-sized Barrow Island males and the larger-sized Dorre Island females. This pattern of introgression was opposite to the expectation that male–male competition or female mate choice would favour larger males. This study shows how mixing diverged populations can bolster genetic variation in newly established mammal populations, but the ultimate outcome can be difficult to predict, highlighting the need for continued genetic monitoring to assess the long-term impacts of admixture. Keywords: burrowing bettong; genetic mixing; intraspecific hybridization; translocation 1. Introduction Species used in conservation translocations are often threatened or rare. Many have isolated populations that are subjected to loss of genetic variation, high levels of inbreeding, and elevated Genes 2019, 10, x; doi: FOR PEER REVIEW www.mdpi.com/journal/genes Genes 2019, 10, x FOR PEER REVIEW 2 of 17 risks of extinction [1–3]. While it has been argued that any threatened populations with unique characteristics or distinct evolutionary history should be conserved separately [4], low genetic diversity and fitness reduction in small populations due to genetic drift and inbreeding can pose significant extinction threats to these populations [5]. Furthermore, an isolated population may accumulate deleterious mutations and have low evolutionary potential in changing environments [6]. For these reasons, translocation programmes involving single source populations may have a high risk of failure. Mixing individuals from different source populations is one way to bolster genetic variation and avoid inbreeding in threatened species [7–9]. Hybridization between diverged populations counteracts the deleterious effects of inbreeding by masking deleterious recessives (dominance) or increasing heterozygosity at loci where heterozygotes have a selective advantage (over-dominance) [10]. A well-known example is the genetic restoration of the Florida panther (Puma concolor coryi). The introduction of Texas panthers (Puma concolor stanleyana) from a geographically nearby population increased genetic diversity, reduced inbreeding, improved survival and fitness, and tripled the number of panthers [11–13]. Furthermore, long-isolated populations often carry different subsets of alleles as a result of lack of gene flow, genetic drift, and local selection [14]. Interbreeding between individuals from these populations should increase evolutionary potential and enable their offspring to survive in a wider range of environments [15,16]. Consistent with this expectation, many translocations sourcing from multiple source populations or genetic rescue cases have shown an increase in genetic diversity and improved fitness over multiple generations [7,17–21]. While mixing differentiated populations can have favourable outcomes, it can also lead to fitness reductions in the progeny (i.e., outbreeding depression) due to post-zygotic isolation between source populations [22–24]. Crossing between phenotypically different parents can produce offspring with phenotypes that are unsuitable for the local environment. For example, a hybridisation of two garter snake populations (Thamnophis ordinoides) produced a mismatch in body pattern and behaviour in hybrid snakes that had a higher mortality from predation in comparison to purebred snakes [25]. Progeny may be unviable because of abnormal structure and/or number of chromosomes [26] or fitness of progeny may be lower due to heterozygote disadvantage, harmful epistatic interaction between alleles of the parents, or disrupting of co-adapted gene complexes [27]. Common signs of intrinsic incompatibility include reduction in fertility and viability of hybrid offspring, such as sterility [26], low survival rate [28], slow growth rate [29], and decreased reproductive success [30]. In addition, pre-zygotic isolation due to differences in morphology, behaviour, ecology, reproductive biology, and gametic compatibility, may prevent or reduce interbreeding between individuals from different source populations [31–33]. This can reduce the effective population size or result in an uneven genetic contribution from the source to the translocated population and induce genetic problems associated with a small population size [34]. Predicting whether outbreeding depression will occur is difficult. Generally, the risk of outbreeding depression becomes higher as the genetic distance between the parents becomes greater, but the amount of divergence required for it to occur varies from species to species [35,36]. The different possible outcomes of mixing diverged populations leave many conservation managers with a difficult decision when choosing populations for use in translocations. This decision can affect the outcome of the translocation and long-term persistence of the population. Allendorf et al. [24] and Edmands [22] suggested that augmenting gene flow between fragmented populations should only be carried out if the populations have lost substantial genetic variation and the effects of inbreeding depression are apparent. However, such information is often not available for populations of immediate conservation concern, and while awaiting data on the effects of inbreeding to be collected, populations are at risk of extirpation. Weeks et al. [37] argued that by overestimating the risk of outcrossing breeding depression, rational use of gene flow for genetic rescue is unnecessarily prevented. So far, a meta-analysis of intentional outcrossing of inbred populations of vertebrates, invertebrates, and plants with a low outbreeding depression risk (evaluated using Frankham et al. 2011 decision tree) has shown positive outcomes of genetic mixing [8], which has lasted for several generations [20]. However, there are only a few case studies available that employed outcrossing for Genes 2019, 10, x FOR PEER REVIEW 3 of 17 conservation purposes [8,9]. Inconsistent outcomes of hybridisation between species, subspecies, and divergent populations and the increasing use of translocation mean that more studies are needed to allow better guidelines about when to use multiple populations in translocation [38]. The boodie or burrowing bettong (Bettongia lesueur) is a medium-sized, burrow-living marsupial endemic to Western Australia. B. lesueur is characterised by a short blunt head, with small rounded and erect ears. They are yellowy grey with a light grey underside, while the legs, feet, and tail are more yellow in colour [39] (Figure 1b). They are omnivorous, nocturnal, and the only macropod that shelters in burrows on a regular basis [39]. The average weight of a Bernier and Dorre Islands boodie is 1.26 ± 13.2 kg [40], in comparison to Barrow Island, which is 0.74 ± 9.2 kg [41] (Figure 1a). The populations on Bernier and Dorre Islands breed throughout the year, peaking over winter when the majority of rain falls [40]. On Barrow Island, breeding cycles are seasonally opposite to Bernier and Dorre islands and peak in summer, coinciding with cyclonic rain [40,41]. Females produce two young on average per year (three maximum) [40]. The young reach sexual maturity after 280 days [40].
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